Destabilization of the Bacterial Interactome Identifies Nutrient Restriction-Induced Dysbiosis in Insect Guts

Marasco, Ramona; Fusi, Marco; Callegari, Matteo; Jucker, Costanza; Mapelli, Francesca; Borin, Sara; Savoldelli, Sara; Daffonchio, Daniele; Crotti, Elena

Abstract

Stress-associated dysbiosis of microbiome can have several configurations that, under an energy landscape conceptual framework, can change from one configuration to another due to different alternating selective forces. It has been proposed—according to the Anna Karenina Principle—that in stressed individuals the microbiome are more dispersed (i.e., with a higher within-beta diversity), evidencing the grade of dispersion as indicator of microbiome dysbiosis. We hypothesize that although dysbiosis leads to different microbial communities in terms of beta diversity, these are not necessarily differently dispersed (within-beta diversity), but they form disrupted networks that make them less resilient to stress. To test our hypothesis, we select nutrient restriction (NR) stress that impairs host fitness but does not introduce overt microbiome selectors, such as toxic compounds and pathogens. We fed the polyphagous black soldier fly, Hermetia illucens, with two NR diets and a control full-nutrient (FN) diet. NR diets were dysbiotic because they strongly affected insect growth and development, inducing significant microscale changes in physiochemical conditions of the gut compartments. NR diets established new configurations of the gut microbiome compared to FN-fed guts but with similar dispersion. However, these new configurations driven by the deterministic changes induced by NR diets were reflected in rarefied, less structured, and less connected bacterial interactomes. These results suggested that while the dispersion cannot be considered a consistent indicator of the unhealthy state of dysbiotic microbiomes, the capacity of the community members to maintain network connections and stability can be an indicator of the microbial dysbiotic conditions and their incapacity to sustain the holobiont resilience and host homeostasis.

Citation

Marasco, R., Fusi, M., Callegari, M., Jucker, C., Mapelli, F., Borin, S., …Crotti, E. (2022). Destabilization of the Bacterial Interactome Identifies Nutrient Restriction-Induced Dysbiosis in Insect Guts. Microbiology Spectrum, 10(1), https://doi.org/10.1128/spectrum.01580-21

• Journal Article Type: Article
• Acceptance Date: Nov 30, 2021
• Online Publication Date: Jan 5, 2022
• Publication Date: 2022-02
• Deposit Date: Feb 1, 2022
• Publicly Available Date: Feb 1, 2022
• Journal: Microbiology Spectrum
• Print ISSN: 2165-0497
• Publisher: American Society for Microbiology
• Peer Reviewed: Peer Reviewed
• Volume: 10
• Issue: 1
• DOI: https://doi.org/10.1128/spectrum.01580-21
• Keywords: nutrient restriction, dysbiosis, bacterial microbiome, beta-diversity, dispersion, black soldierfly, interactome, co-occurrence network, gut, keystone species
• Public URL: http://researchrepository.napier.ac.uk/Output/2839636